Predation by Snakes Thwarts Trial Reintroduction of the Endangered Woma Python Aspidites Ramsayi J

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Predation by snakes thwarts trial reintroduction of the Endangered woma python Aspidites ramsayi J. L. Read,G.R.Johnston and T. P. Morley

Abstract Case studies of well-documented snake reintro- species (Dodd, 1987, 1993; Reinert, 1991) has hindered the ductions are limited, despite their potential value for implementation of snake reintroductions. conservation and ecosystem recovery. The Endangered Experimental evidence suggests that translocated snakes woma Aspidites ramsayi is a large boid snake that has move further, more erratically and exhibit lower survivor- declined considerably and is now threatened throughout ship than resident snakes (Fitch & Shirer, 1971; Landreth, much of central Australia. We describe a trial release of 1973; Galligan & Dunson, 1979; Reinert & Rupert, 1999; captive-bred womas into the feral predator-free Arid Re- Plummer & Mills, 2000; Butler et al., 2005). Behavioural covery Reserve in northern South Australia. All of the changes that decrease survivorship of translocated snakes reintroduced womas were killed within 4 months, with are accentuated for captive-bred individuals that may be predation by the mulga snake Pseudechis australis con- less efficient at feeding or locating suitable refuges than firmed or implied in all cases. Lessons learned for the wild-caught relocated animals (Plummer & Mills, 2000; conditioning of captive-bred snakes for wild release and Mathews et al., 2005). Reintroduction success of captive- the role of the mulga snake in structuring Australian arid- bred snakes is therefore likely to be enhanced where prey zone snake assemblages are discussed. populations are high, snake movements are contained, refuge sites from predators are plentiful and temperature Keywords Arid zone, Aspidites ramsayi, Australia, elapid, extremes are limited. predation, python, reintroduction, woma The woma Aspidites ramsayi is an Australian boid snake that is thought to have declined because of habitat clearing in mesic environments and predation by feral domestic cats Introduction Felis catus and foxes Vulpes vulpes (Wilson & Knowles, 1988; Pearson, 1993; Maryan, 2002). Although aborigines eintroductions are widely recognized as integral to also hunt womas (Baker et al., 1993; Read, 2003) there is no many species’ conservation and ecosystem recovery R evidence that this hunting has contributed to their decline. initiatives (Fischer & Lindenmayer, 2000; Seddon et al., Predation by cats and foxes in concert with other factors 2007), despite most efforts failing to establish viable has been implicated in driving many of the native mam- populations (Griffith et al., 1989; Dodd & Seigel, 1991;Beck malian prey species of womas to extinction or serious et al., 1994; Wolf et al., 1996). Despite playing an important decline in the Australian arid zone (Johnson, 2006; role as predators in many environments and improved McKenzie et al., 2007) and hence may represent both success rates for recent reintroductions (Germano & a direct and indirect threat to woma populations. Predation Bishop, 2009), snake reintroductions are underrepresented by dingoes Canis lupus dingo, or dogs Canis lupus familiaris in conservation management (Seddon et al., 2005). This has been significant for other arid-zone pythons (Heard paucity of snake reintroductions may be attributed to the et al., 2004) and hence could be a factor. The long-term low public interest in reptile conservation relative to birds viability of conservation programmes in degraded environ- and mammals. Furthermore, although comprehensive nat- ments is compromised by re-establishment of a single ural history or conservation status information has been threatened species in comparison to the recreation of more integral to the success of two well-documented snake sustainable functioning ecosystems in which populations reintroductions (Tolson & Garcia, 1997; Daltry et al., of reintroduced species are both enhanced and limited 2001) the lack of such information for many snake by biological factors (Seddon et al., 2007; Armstrong & Seddon, 2008). Optimal conservation management and reintroduction sites for the woma should therefore experi- J.L. READ (Corresponding author) Arid Recovery, G.P.O. Box 150, Roxby Downs, South Australia 5725, Australia, and School of Earth and Environ- ence nil or low cat, fox and dog predation and support as mental Sciences, University of Adelaide, Adelaide, South Australia, Australia. many of the natural potential prey species and ecosystem E-mail [email protected] drivers as possible. G.R. JOHNSTON School of Biological Sciences, Flinders University of South Australia, Adelaide, South Australia, Australia, and Zoos South Australia, Here we describe an experimental reintroduction of Adelaide, South Australia, Australia captive-bred womas. Because the only available release

T.P. MORLEY Zoos South Australia, Adelaide, South Australia, Australia animals were siblings, this reintroduction was considered Received 19 April 2010. Revision requested 17 June 2010. a trial of the appropriateness of habitats, food availability, Accepted 7 July 2010. First published online 31 August 2011. predator density and use of captive-bred pythons, rather

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than a genetically-robust reintroduction. Womas were ecosystem recovery and reintroductions to the Reserve. released at a South Australian arid-zone site where in- Recovery of mammal populations at the Arid Recovery troduced predators had been excluded and the native Reserve has occurred through natural increases following mammal fauna, including four successfully reintroduced removal of introduced mammals (Moseby et al., 2009), and species (greater stick-nest rat Leporillus conditor, burrow- the successful reintroduction of locally extinct mammal ing bettong Bettongia lesueur, greater bilby Macrotis lagotis species, including the bilby and another medium-sized and western barred bandicoot Parameles bougainville) had burrowing species, the burrowing bettong (Read et al., made some recovery. 2008). In addition to developing a reintroduction protocol to improve the conservation status of womas, introduction Methods of a native predator is an appropriate management initia- tive to limit burgeoning mammal populations within the The woma python Arid Recovery Reserve and to assist with the restoration of sustainable ecosystem processes. The woma is a large (# 3.0 m) terrestrial python endemic to arid and semi-arid Australia. Womas are primarily Origin of the stock and captive husbandry nocturnal although they may occasionally be active by day (Fyfe & Harvey, 1981; Maryan, 2002), and they have Ten captive-bred sibling womas derived from wild stock a catholic diet that includes rodents, bandicoots, other obtained close to the release site were chosen for the trial snakes, a variety of lizards, and birds (Fyfe & Harvey, 1981; reintroduction. We considered regional provenance to be Shine & Slip, 1990; Tyler et al., 1990; Covacevich & Couper, important because the woma exhibits considerable geo- 1996). Historically, womas made extensive use of bilby graphical variation in morphology (Morley, 1999). The holes for shelter, and probably preyed on bilbies, resulting dam and sire were donated to Adelaide Zoo from the in the colloquial name bilby snake (Covacevich & Couper, Moomba area (280609 S, 140119 E) and a road north of 1996). Following the reduction of native Australian burrow- the Flinders Ranges, respectively. The sire was placed in the ing mammals (Johnson, 2006) womas are known to same enclosure as the dam at Adelaide Zoo on 12 April 2002 have utilized warrens of introduced rabbits Oryctolagus and mating was observed on 27 April 2002. Eighteen eggs cuniculus (GRJ & JLR, unpubl. data). Despite this adapta- were laid on 3 October 2002. Thirteen of the eggs hatched tion, woma abundance and distribution have declined to successfully but three of the resulting neonates subsequently the extent that, notwithstanding the IUCN Red List died. Neonates weighed 16.6–52.3 g (mean 40.4 – SE 12.0 g) categorization of the species as Endangered (Australasian and total lengths were 381–465 mm (mean 414 – SE 37 mm). Marsupial & Monotreme Specialist Group, 1996), it is The captive husbandry practices for womas at Adelaide Zoo categorized as Critically Endangered in southern Western have been described in detail by Morley (1999). Individual Australia (Cogger et al., 1993; Maryan, 2002), and Endan- womas were identified using microchips (Trovan, Douglas, gered or Vulnerable elsewhere in its range (Hutchinson, UK) placed under the skin on the left-hand side, just anterior 1992; Sadlier, 1994; Covacevich & Couper, 1996). to the cloaca. Miniature radio-transmitters (SI-2, Holohil, Canada) 3 5 The release site were surgically implanted into the gut cavity on – April 2007. Surgical implantation of transmitters typically does 2 The Arid Recovery Reserve is a 60 km fenced exclosure in not affect the health or behaviour of snakes (Slip & Shine, northern South Australia (30299 S, 136539 E) from which 1988; Madsen & Shine, 1996; Heard et al., 2004). Each all rabbits, cats and foxes have been removed (Moseby & transmitter weighed 11 g, was 40 3 11 mm with a 200 mm Read, 2006). Main habitats within the Reserve are linear Teflon-coated antenna and a nominal life of 12–24 months. orange sand dunes, vegetated by Acacia spp., Dodonaea A 20–30 mm para-ventral incision was made 85–90% of the viscosa and Zygochloa paradoxa, separated by sandy or snout-vent length (SVL) from the snout under general stony clay swales vegetated by low chenopod shrubland. anaesthesia using isoflourane. Transmitters were inserted The Reserve lies within the known historical natural range into the gut cavity cranially and antennae inserted caudal to of the woma. Road-killed womas have been collected 25 km the incision. The gut cavity wall, muscle and skin were south of the Arid Recovery Reserve on 10 October 1990 sutured with coated vicryl. Antibiotics (Batryl/Enrofloxan, (South Australian Museum R41841) and 150 km north-west Bayer Corp., Leverkusen, Germany) were applied subcuta- 1 of the Reserve (30 km east of William Creek) on 25 neously at a dose of 10 mg kg- in a 1 : 5 saline solution every February 2002. The failure of many attempts to reintroduce 48 h seven times following implantation. On the day of threatened Australian mammals has been attributed to surgery snakes weighed 850–1,308 g (mean 1,032 – SE 140 g) predation by introduced predators (Short et al., 1992), and had SVLs of 1,210–1,400 mm (mean 1,312 – SE 58 mm). hence the removal of cats and foxes has been integral to All snakes fed and sloughed their skin at least once following

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transmitter insertion before they were released. One trans- Reintroduction and monitoring mitter failed and therefore only nine animals were released. 890 1 353 Prior to the release the incidence of endemic parasites Two female and seven male womas, weighing – , g 1 020 140 and potential pathogens was investigated in reptiles from (mean 5 , – SE g), were transported in calico bags the Arid Recovery Reserve. During January–October 2005 inside foam boxes from Adelaide Zoo to Roxby Downs on 21 2007 23 individuals of seven species of lizard and two species of September . The success of womas released directly 1 4 snake were investigated using cloacal swabs for bacteriology into the Arid Recovery Reserve (‘hard’ release; $ #) was and faecal parasitology, and blood samples from live intended to be compared with individuals released in a pen 1 3 0 5 animals or histopathology following post mortem exami- within the Reserve (‘soft’ release; $ #). The . ha pen was 900 10 nation of road-kill specimens (Table 1). All womas identi- surrounded by a -mm high fence of -mm diameter ﬁed for release were held in isolation from all other reptiles wire netting into which non-viable, weed-free oats were 5 from May 2004 until release in September 2007. In addition spread for weeks before the release and weekly thereafter to quarantining this extended period in captivity was to encourage high rodent densities, principally Notomys designed to grow the pythons to a size where predation alexis, Pseudomys bolami and Mus musculus. However, by potential native predators (mulga or king brown snake all four womas breached the release-pen fence within 2 Pseudechis australis, Gould’s goanna Varanus gouldii, months and hence comparisons of release techniques brown falcon Falco berigora and wedge-tailed eagle Aquila were abandoned. audax) was less likely and the range of potential food items Each woma was released adjacent to a disused bilby 22 2007 was increased. During this time they exhibited no symp- burrow on the morning of September . Released 4 toms of disease. We paid particular attention to the womas were observed for up to hours until they had possibility of ophidian paramyxovirus or inclusion body retreated to shelter, generally a burrow. Following release disease. All released snakes were negative for DNA tests for the womas were radio-tracked daily to determine their paramyxovirus. location, habitat, health and details of retreats used. We

TABLE 1 Endemic pathogens and parasites recorded from reptiles collected in the vicinity of the Arid Recovery Reserve (Fig. 1), where the womas were subsequently released. Species (by Family) n Test Result Agamidae Ctenophorus nuchalis 3 Blood smears Nil Pogona vitticeps 2 Blood smears ?Haemoproteus sp. in one animal Tympanocryptis intima 4 Blood smears Nil Gekkonidae Diplodactylus conspicillatus 2 Blood smears Nil Scincidae Ctenotus regius 2 Blood smear Nil Tiliqua rugosa 1 Cloacal swab Nil Varanidae Varanus gouldii 3 Cloacal swab Nil Histopathology Unidentified ticks & nematodes Cloacal swab Nil Histopathology Nil Cloacal swab Salmonella; heavy growth of E. coli and Salmonella spp. Histopathology Unidentified ticks & nematodes Elapidae Pseudonaja sp. 4 Cloacal swab Heavy growth of Pseudomonas aeroginosa Histopathology Multiple duodenal ulcers associated with embedded unidentified nematodes Blood smear Nil Cloacal swab Salmonella Chester Pseudechis australis 2 Cloacal swab Heavy growth of P. aeroginosa

deliberately located snakes at different times of the day to maximize the diurnal range of observations but found that we were not able to locate nocturnal ﬁxes with precision or conﬁdence without potentially damaging the refuges. Therefore most radio-tracking was conducted during day- light hours. Any tracks of womas and other animals found within 1 m of each woma shelter site were recorded when weather conditions permitted, allowing interpretation of woma activity patterns and potential prey or predator interactions. Following each visit to a refuge site all traces were obliterated by sweeping the sand so that woma and PLATE 1 Mulga snake Pseudechis australis biting a reintroduced other animal activity could be assessed on a daily basis. woma Aspidites ramsayi at the Arid Recovery Reserve in South Australia (Fig. 1). Photograph: Chris McGoldrick. Statistical analysis

The distances travelled by womas and any mulga snakes With the exception of moribund animals that had that subsequently consumed them were compared using recently been attacked by mulga snakes, none of the womas the Mann–Witney U test to explore the nature of potential appeared emaciated or unhealthy whenever they were interactions between the species. A mixed model two-way observed directly during the trial. Successful feeding was ANOVA was used to compare the frequency with which confirmed for #91, which contained substantial fat bodies tracks of different animals were recorded near woma during necropsy following its death 101 days after release. 2 refuges. A v test was used to compare refuges (burrows, When captured 77 days after its initial release #94 had lost under vegetation, open surface) used by womas with that 24% of its release mass. Despite this loss it defecated, expected under a random distribution. All statistics were suggesting it had fed since being released. Animal #95 lost calculated using SPSS v. 15.0 (SPSS, Chicago, USA). 27% of its release weight after 112 days and a further 10% over the next 11 days until it was killed but was not Results considered to be emaciated upon necropsy. All womas remained in their initial shelter for 6–52 days The most noteworthy outcome of this study was that all (mean 5 28 – SE 19 days, n 5 9). On several occasions dur- released woma pythons were dead between 41 and 123 days ing this initial sedentary period individuals were observed following release, either definitely or most likely killed by near the entrance of the shelter or short tracks were observed, mulga snakes. Three python mortalities were attributed to suggesting the snakes may have been basking. Womas were at least two, probably three, different mulga snakes. Two of located 38–99 times following release (mean 5 68 – SE these womas were eaten by different mulga snakes that 19 days, n 5 9). Following an initial sedentary period the continued to be radio-tracked until they excreted their womas moved shelters on average every 5.2 days (2.9–8.8 transmitters 33 and 23–27 days later. The other woma (#98) days) and individuals travelled a mean minimum distance of was observed being repeatedly struck and dragged around 15–227 m between consecutive refuges. Woma pythons by a mulga snake but was not swallowed (Plate 1). Three moved significantly shorter minimum distances (109 – SE other womas were most likely killed by mulga snakes that 20 m, n 5 68) than three radio-tracked mulga snakes (243 – were observed entering woma burrows immediately before SE 80 m, n 5 13; Mann–Whitney U 5 281,P5 0.033). their death (#97) or they were located near death or dead Of the 68 woma shelter sites located, 35 (51%) were on with severe bruising and/or heart and lung damage con- dune crests, 32 (47%) were on dune flanks and one was on sistent with mulga snake envenomation (#91 and #95). Two a swale adjacent to a dune base (Fig. 1). The snakes also other womas (#93 `) were removed from burrows in showed a clear pattern in the kind of refuge they used 2 a decomposed state several days after many snake tracks (v2 5 74.9,P5 0.000). Fifty-six (82%) shelter sites were were observed at the burrow, consistent with the sign left by burrows or warrens, 10 (15%) were in undergrowth, mainly a confirmed mulga snake attack followed by regurgitation canegrass Zyglochoa paradoxa, and two (3%) were un- of the woma. The final woma transmitter (#99) was lost derground with no burrow evident. Burrows used included after it had moved widely on a swale for several days five hopping mouse Notomys alexis pop holes c. 60 mm in without being sighted, which was consistent with the diameter, six goanna burrows c. 135 3 75 mm in size, and 25 movements of both mulga snakes known to have consumed were bilby or bettong burrows, typically with a burrow womas (see below). We assume that this woma was entrance of 200–250 3 150 mm. swallowed by a mulga snake shortly before the long- There were significant differences in potential dietary distance movements of its transmitter commenced. species’ tracks recorded at woma refuges (F4,28 5 49.884,

FIG. 1 Map of part of the Arid Recovery Reserve showing locations where nine woma pythons Aspidites ramsayi (#91–99), and subsequently mulga snakes Pseudechis australis that predated three pythons, were found.

P 5 0.000), with rodent tracks (70.4 – SE 3.8%) occurring feral cats and foxes posed the main risk for woma pythons more frequently than all other kinds of tracks (Fig. 2). This and that their removal would have facilitated the woma suggests that womas in both release groups had access to reintroduction, as it had for the successful reintroduction of ample potential prey. four mammal species vulnerable to predation. We also incorrectly assumed, based on the work of King & Stanford 2006 Discussion ( ), that we had minimized the potential for predation by raptors and large reptiles to thwart the woma reintro- The key outcome of this trial release was that captive-bred duction by waiting for the womas to reach in excess of 850 g womas were rapidly eaten or killed by mulga snakes when before release. King & Stanford (2006) found that plains released into the wild. This finding presents a significant garter snakes Thamnophis radix incubated and raised challenge for snake reintroductions wherever mulga snakes in captivity exhibited greater survival, particularly when occur in arid and tropical Australia. Predation by native or released as large snakes, compared to wild-hatched garter introduced predators is a key contributing factor to many snakes. reintroduction failures (Short et al., 1992; Griffin et al., Further research with reintroduced predator-trained 2000). Prior to this study we assumed that predation by captive snakes, relocated wild snakes and in situ snake

Future reintroduction of womas, and potentially other pythons, to regions inhabited by mulga snakes, should consider reducing their vulnerability by using larger individuals accustomed to predators, either wild-raised or trained. Mulga snake densities could also be reduced during the initial phase of the reintroduction, although the estimation of actual, natural or appropriate mulga snake densities is problematical because of their cryptic nature and long periods of inactivity. The high incidence of deaths inflicted by mulga snakes, FIG. 2 Percentage of days that tracks of snakes (including which are relatively abundant and widespread across much womas), rodents, bilbies Macrotis lagotis, burrowing bettongs Bettongia lesueur, goannas Varanus gouldii and small lizards of arid and tropical Australia, raises a number of questions were recorded in or immediately adjacent to occupied refuges of about snake ecology in arid Australia. Given that mulga ‘hard’ and ‘soft’ released (see text for details) womas. snakes are widespread and typically abundant throughout much of mainland Australia, what role does their predation or envenomation play in structuring snake assemblages and populations is required to determine whether the what conditions are necessary for successful recruitment of 2 vulnerability of womas to mulga snakes reported here vulnerable species? Although cats kill c. 700 lizards km- indicate that mulga snakes significantly limit wild woma each year in the Roxby region (Read & Bowen, 2001), populations. Alternative hypotheses for the high predation secondary trophic relationships, including an increase in include the naivety of the captive-bred snakes to predators varanids following removal of foxes and cats, may have or that mulga snake abundance or behaviour within the contributed even more to the reduced reptile abundance Arid Recovery Reserve during the trial release was atypical. apparent within the Arid Recovery Reserve (Moseby et al., Pre-release training has the potential to enhance the 2009; Read & Cunningham, 2010). Our study raises the expression of pre-existing anti-predator behaviour in cap- possibility that mulga snakes may also be contributing to tive bred animals (Miller et al., 1990; McLean et al., 1996; the suppression of reptile, especially other snake, popula- Griffin et al., 2000). Often this training involves learning tions in the Reserve. In at least five of the nine mulga snake/ from the behaviour of conspecifics (Curio, 1988; Mineka & woma interactions the mulga swallowed the woma and Cook, 1988). Perhaps because reptiles are seldom social and hence predation was probably the key motivation for the do not exhibit maternal care, pre-release training and post- killing. However, at least two of the womas were killed by release provisioning is less commonly used for reptile mulga snakes but not swallowed. These cases may represent reintroductions compared to those of mammals or birds failed predation attempts because the prey proved to be too (Beck et al., 1994; Griffith et al., 1989). large. The death rate may therefore have been reduced had The vulnerability of the reintroduced woma pythons to more pythons been translocated and the local mulga predation was perhaps accentuated by their inexperience snakes, which had not previously encountered reptilian with feeding and seeking optimal refuges. Captive-bred prey too large to swallow, learned their limitations. Alter- animals may be less efficient at capturing prey than wild- natively, the mulga snakes may have attacked the womas caught animals (Mathews et al., 2005). For instance, because they perceived them to be either a direct threat or captive-bred hognose snakes Heterodon platirhinos expe- potential competitors. rienced higher mortalities than wild-raised individuals because of failure to find appropriate hibernation sites 2000 (Plummer & Mills, ). Acknowledgements Although lessons learned from both successful and failed translocations are integral to improving applied Arid Recovery partners and staff are thanked for their conservation management, many potentially valuable re- support and provision of the landscape-scale reintro- introduction attempts have not been documented in the duction and research site. Zoos South Australia staff are peer-reviewed scientific literature (Fischer & Lindenmayer, acknowledged for breeding, husbandry and veterinary 2000). Deficiencies in documenting reintroduction perfor- work. Friends of Arid Recovery and Zoowatch volunteers mance is biased towards birds and mammals (Bajomi et al. (particularly Jennifer Hayes), and staff of Arid Recovery 2009), thus increasing the value of reptile case studies. This and Zoos South Australia assisted with post-release mon- woma reintroduction study revealed that intensively monitoring. Helen Crisp prepared Fig. 1. Dave Pearson and itored trial releases can provide valuable information on the anonymous referees provided constructive criticism. natural history of the target species and also improve Funding was provided by the Royal Zoological Society methods for successful establishment of new populations. of South Australia, the Arid Recovery Project, the

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